Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis

  1. Michael Borg
  2. Ranjith K Papareddy
  3. Rodolphe Dombey
  4. Elin Axelsson
  5. Michael D Nodine
  6. David Twell
  7. Frédéric Berger  Is a corresponding author
  1. Gregor Mendel Institute, Austria
  2. University of Leicester, United Kingdom

Abstract

Alternation between morphologically distinct haploid and diploid life forms is a defining feature of most plant and algal life cycles, yet the underlying molecular mechanisms that govern these transitions remain unclear. Here, we explore the dynamic relationship between chromatin accessibility and epigenetic modifications during life form transitions in Arabidopsis. The diploid-to-haploid life form transition is governed by the loss of H3K9me2 and DNA demethylation of transposon-associated cis-regulatory elements. This event is associated with dramatic changes in chromatin accessibility and transcriptional reprogramming. In contrast, the global loss of H3K27me3 in the haploid form shapes a chromatin accessibility landscape that is poised to re-initiate the transition back to diploid life after fertilization. Hence, distinct epigenetic reprogramming events rewire transcription through major reorganization of the regulatory epigenome to guide the alternation of generations in flowering plants.

Data availability

Deep-sequencing data that support the findings of this study have been deposited in the Gene Expression Omnibus (GEO) under accession code GSE155369. Re-analysis of previously published DNA methylomes from dme-2/+ pollen (Ibarra et al., 2012), and siRNAs from leaves (Papareddy et al., 2020) and pollen (Borges et al., 2018; Slotkin et al., 2009) were deposited in the GEO under accession code GSE155369.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Michael Borg

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3982-3843
  2. Ranjith K Papareddy

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Rodolphe Dombey

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3670-4128
  4. Elin Axelsson

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4382-1880
  5. Michael D Nodine

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. David Twell

    Department of Genetics, University of Leicester, Leicester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Frédéric Berger

    Gregor Mendel Institute, Vienna, Austria
    For correspondence
    Frederic.berger@gmi.oeaw.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3609-8260

Funding

Austrian Science Fund (P26887)

  • Frédéric Berger

Austrian Science Fund (I 4258)

  • Frédéric Berger

Austrian Science Fund (I2163-B16)

  • Frédéric Berger

Austrian Science Fund (M1818)

  • Michael Borg

European Commission (ERC 637888)

  • Michael D Nodine

Biotechnology and Biological Sciences Research Council (BB/I011269/1)

  • David Twell

Biotechnology and Biological Sciences Research Council (BB/N005090)

  • David Twell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Richard Amasino, University of Wisconsin Madison, United States

Version history

  1. Received: August 7, 2020
  2. Accepted: January 25, 2021
  3. Accepted Manuscript published: January 25, 2021 (version 1)
  4. Version of Record published: March 1, 2021 (version 2)

Copyright

© 2021, Borg et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Michael Borg
  2. Ranjith K Papareddy
  3. Rodolphe Dombey
  4. Elin Axelsson
  5. Michael D Nodine
  6. David Twell
  7. Frédéric Berger
(2021)
Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis
eLife 10:e61894.
https://doi.org/10.7554/eLife.61894

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